Winter chilling speeds spring development of temperate butterflies

Abstract

Understanding and predicting phenology has become more important with ongoing climate change and has brought about great research efforts in the recent decades. The majority of studies examining spring phenology of insects have focussed on the effects of spring temperatures alone. Here we use citizen-collected observation data to show that winter cold duration, in addition to spring temperature, can affect the spring emergence of butterflies. Using spatial mixed models, we disentangle the effects of climate variables and reveal impacts of both spring and winter conditions for five butterfly species that overwinter as pupae across the UK, with data from 1976 to 2013 and one butterfly species in Sweden, with data from 2001 to 2013. Warmer springs lead to earlier emergence in all species and milder winters lead to statistically significant delays in three of the five investigated species. We also find that the delaying effect of winter warmth has become more pronounced in the last decade, during which time winter durations have become shorter. For one of the studied species, Anthocharis cardamines (orange tip butterfly), we also make use of parameters determined from previous experiments on pupal development to model the spring phenology. Using daily temperatures in the UK and Sweden, we show that recent variation in spring temperature corresponds to 10-15 day changes in emergence time over UK and Sweden, whereas variation in winter duration corresponds to 20 days variation in the south of the UK versus only 3 days in the south of Sweden. In summary, we show that short winters delay phenology. The effect is most prominent in areas with particularly mild winters, emphasising the importance of winter for the response of ectothermic animals to climate change. With climate change, these effects may become even stronger and apply also at higher latitudes.

Multiple temperature effects on phenology and body size in wild butterflies predict a complex response to climate change

“…This work complements studies investigating the general responses of butterflies to climate change across space and time (e.g., Phillimore et al 2012, Brooks et al 2014, Fenberg et al 2016, and the specific responses of A. cardamines to temperature changes in the laboratory (St alhandske et al 2014(St alhandske et al , 2015(St alhandske et al , 2017. This work complements studies investigating the general responses of butterflies to climate change across space and time (e.g., Phillimore et al 2012, Brooks et al 2014, Fenberg et al 2016, and the specific responses of A. cardamines to temperature changes in the laboratory (St alhandske et al 2014(St alhandske et al , 2015(St alhandske et al , 2017.…”

“…The retardation of emergence with increasing November temperatures can be explained on the assumption that winter chilling is required to break pupal diapause (St alhandske et al 2015(St alhandske et al , 2017, and hence higher November temperatures delay the onset of this process (a retardation in the peak flight date of A. cardamines with increasing November temperatures was also reported by Roy and Sparks [2000]). The effect of June-July temperatures during late larval and/or early pupal life implies either that the developmental point reached at diapause is variable and temperature dependent, or that postdiapause development is faster in specimens that have been exposed to warmer prediapause temperatures.…”

“…The former possibility would invalidate the assumption that development is synchronized during winter in pupal diapausing species (Wiklund and Forsberg 1991) and merits further investigation. The retardation of emergence with increasing November temperatures can be explained on the assumption that winter chilling is required to break pupal diapause (St alhandske et al 2015(St alhandske et al , 2017, and hence higher November temperatures delay the onset of this process (a retardation in the peak flight date of A. cardamines with increasing November temperatures was also reported by Roy and Sparks [2000]). The advancement of emergence with increasing spring temperatures can be attributed to the direct effect of temperature on postdiapause development rate.…”

“…I here examine the phenological and body-size responses of A. cardamines to temperatures operating over the entire life span of the organism in a wild population over 14 generations. This work complements studies investigating the general responses of butterflies to climate change across space and time (e.g., Phillimore et al 2012, Brooks et al 2014, Fenberg et al 2016, and the specific responses of A. cardamines to temperature changes in the laboratory (St alhandske et al 2014(St alhandske et al , 2015(St alhandske et al , 2017. I also investigate the effect of temperature on the flowering time of the butterfly's two main host plants, to determine if unequal phenological shifts between trophic levels could develop as a consequence of global warming.…”

“…In the univoltine orange-tip butterfly, Anthocharis cardamines, increased exposure to cold in the laboratory leads to decreased postwinter pupal development time and earlier and more synchronized emergence of the adults (St alhandske et al 2015). This has important implications for interpreting the apparent countergradient emergence pattern of this species across the United Kingdom (UK; Phillimore et al 2012); in southern England, individuals emerge later than predicted solely on the basis of high spring temperatures due to short winter durations (St alhandske et al 2015(St alhandske et al , 2017. This emphasizes the need to assess the impact of temperature across the entire pupal period for species that overwinter in this stage.…”